SlMYB99-mediated auxin and abscisic acid antagonistically regulate ascorbic acids biosynthesis in tomato.


Journal

The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884

Informations de publication

Date de publication:
08 2023
Historique:
received: 30 01 2023
accepted: 28 04 2023
medline: 30 6 2023
pubmed: 29 5 2023
entrez: 29 5 2023
Statut: ppublish

Résumé

Ascorbic acid (AsA) is a water-soluble antioxidant that plays important roles in plant development and human health. Understanding the regulatory mechanism underlying AsA biosynthesis is imperative to the development of high AsA plants. In this study, we reveal that the auxin response factor SlARF4 transcriptionally inhibits SlMYB99, which subsequently modulates AsA accumulation via transcriptional activation of AsA biosynthesis genes GPP, GLDH, and DHAR. The auxin-dependent transcriptional cascade of SlARF4-SlMYB99-GPP/GLDH/DHAR modulates AsA synthesis, while mitogen-activated protein kinase SlMAPK8 not only phosphorylates SlMYB99, but also activates its transcriptional activity. Both SlMYB99 and SlMYB11 proteins physically interact with each other, thereby synergistically regulating AsA biosynthesis by upregulating the expression of GPP, GLDH, and DHAR genes. Collectively, these results demonstrate that auxin and abscisic acid antagonistically regulate AsA biosynthesis during development and drought tolerance in tomato via the SlMAPK8-SlARF4-SlMYB99/11 module. These findings provide new insights into the mechanism underlying phytohormone regulation of AsA biosynthesis and provide a theoretical basis for the future development of high AsA plants via molecular breeding.

Identifiants

pubmed: 37247338
doi: 10.1111/nph.18988
doi:

Substances chimiques

Abscisic Acid 72S9A8J5GW
Indoleacetic Acids 0
Ascorbic Acid PQ6CK8PD0R
Antioxidants 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

949-963

Informations de copyright

© 2023 The Authors. New Phytologist © 2023 New Phytologist Foundation.

Références

An JP, Wang XF, Zhang XW, Xu HF, Bi SQ, You CX, Hao YJ. 2020. An apple MYB transcription factor regulates cold tolerance and anthocyanin accumulation and undergoes MIEL1-mediated degradation. Plant Biotechnology Journal 18: 337-353.
Bouzroud S, Gasparini K, Hu G, Barbosa MAM, Rosa BL, Fahr M, Bendaou N, Bouzayen M, Zsögön A, Smouni A et al. 2020. Down regulation and loss of auxin response factor 4 function using CRISPR/Cas9 alters plant growth, stomatal function and improves tomato tolerance to salinity and osmotic stress. Genes 11: 272.
Carr AC, Maggini S. 2017. Vitamin C and immune function. Nutrients 9: 121.
Chen G, Zheng D, Feng N, Zhou H, Mu D, Zhao L, Shen X, Rao G, Meng F, Huang A. 2022. Physiological mechanisms of ABA-induced salinity tolerance in leaves and roots of rice. Scientific Reports 12: 8228.
Chen Y, Shu P, Wang R, Du X, Xie Y, Du K, Deng H, Li M, Zhang Y, Grierson D et al. 2021. Ethylene response factor AcERF91 affects ascorbate metabolism via regulation of GDP-galactose phosphorylase encoding gene (AcGGP3) in kiwifruit. Plant Science 313: 111063.
Cross TG, Scheel-Toellner D, Henriquez NV, Deacon E, Salmon M, Lord JM. 2000. Serine/threonine protein kinases and apoptosis. Experimental Cell Research 256: 34-41.
Deng W, Yang YW, Ren ZX, Audran-Delalande C, Mila I, Wang XY, Song HL, Hu YH, Bouzayen M, Li ZG. 2012. The tomato SlIAA15 is involved in trichome formation and axillary shoot development. New Phytologist 194: 379-390.
Emenecker RJ, Strader LC. 2020. Auxin-abscisic acid interactions in plant growth and development. Biomolecules 10: 281.
Fu DQ, Zhu BZ, Zhu HL, Jiang WB, Luo YB. 2005. Virus-induced gene silencing in tomato fruit. The Plant Journal 43: 299-308.
Hasanuzzaman M, Bhuyan MHMB, Anee TI, Parvin K, Nahar K, Mahmud JA, Fujita M. 2019. Regulation of ascorbate-glutathione pathway in mitigating oxidative damage in plants under abiotic stress. Antioxidants 8: 384.
Hu G, Wang K, Huang B, Mila I, Frasse P, Maza E, Djari A, Hernould M, Zouine M, Li Z et al. 2022. The auxin-responsive transcription factor SlDOF9 regulates inflorescence and flower development in tomato. Nature Plants 8: 419-433.
Hu T, Ye J, Tao P, Li H, Zhang J, Zhang Y, Ye Z. 2016. The tomato HD-Zip I transcription factor SlHZ24 modulates ascorbate accumulation through positive regulation of the d-mannose/l-galactose pathway. The Plant Journal 85: 16-29.
Huang B, Hu G, Wang K, Frasse P, Maza E, Djari A, Deng W, Pirrello J, Burlat V, Pons C et al. 2021. Interaction of two MADS-box genes leads to growth phenotype divergence of all-flesh type of tomatoes. Nature Communications 12: 6892.
Ishikawa T, Maruta T, Yoshimura K, Smirnoff N. 2018. Biosynthesis and regulation of ascorbic acid in plants. In: Gupta DK, Palma JM, Corpas FJ, eds. Antioxidants and antioxidant enzymes in higher plants. Cham, Switzerland: Springer, 163-179.
Li F, Li M, Wang P, Cox KL, Jr Duan L, Dever JK, Shan L, Li Z, He P. 2017. Regulation of cotton (Gossypium hirsutum) drought responses by mitogen-activated protein (MAP) kinase cascade-mediated phosphorylation of GhWRKY59. New Phytologist 215: 1462-1475.
Liu X, Wu R, Bulley SM, Zhong C, Li D. 2022. Kiwifruit MYBS1-like and GBF3 transcription factors influence l-ascorbic acid biosynthesis by activating transcription of GDP-l-galactose phosphorylase 3. New Phytologist 234: 1782-1800.
Liu X, Zhang H, Zhao Y, Feng Z, Li Q, Yang HQ, Luan S, Li J, He ZH. 2013. Auxin controls seed dormancy through stimulation of abscisic acid signaling by inducing ARF-mediated ABI3 activation in Arabidopsis. Proceedings of the National Academy of Sciences, USA 110: 15485-15490.
Macknight RC, Laing WA, Bulley SM, Broad RC, Johnson AAT, Hellens RP. 2017. Increasing ascorbate levels in crops to enhance human nutrition and plant abiotic stress tolerance. Current Opinion in Biotechnology 44: 153-160.
Miret JA, Munné-Bosch S. 2016. Abscisic acid and pyrabactin improve vitamin C contents in raspberries. Food Chemistry 203: 216-222.
Mohammadi F, Naghavi MR, Peighambari SA, Khosravi Dehaghi N, Khaldari I, Bravi E, Marconi O, Perretti G. 2021. Abscisic acid crosstalk with auxin and ethylene in biosynthesis and degradation of inulin-type fructans in chicory. Plant Biology 23: 636-642.
Moser MA, Chun OK. 2016. Vitamin C and heart health: a review based onfindings from epidemiologic studies. International Journal of Molecular Sciences 17: 132.
Perin EC, da Silva MR, Borowski JM, Crizel RL, Schott IB, Carvalho IR, Rombaldi CV, Galli V. 2019. ABA-dependent salt and drought stress improve strawberry fruit quality. Food Chemistry 271: 516-526.
Pullar JM, Carr AC, Vissers MCM. 2017. The roles of vitamin C in skin health. Nutrients 9: 866.
Qin G, Wang Y, Cao B, Wang W, Tian S. 2012. Unraveling the regulatory network of the MADS box transcription factor RIN in fruit ripening. The Plant Journal 70: 243-255.
Qin J, Zhao C, Wang S, Gao N, Wang X, Na X, Wang X, Bi Y. 2022. PIF4-PAP1 interaction affects MYB-bHLH-WD40 complex formation and anthocyanin accumulation in Arabidopsis. Journal of Plant Physiology 268: 153558.
Qiu Y, Tao R, Feng Y, Xiao Z, Zhang D, Peng Y, Wen X, Wang Y, Guo H. 2021. EIN3 and RSL4 interfere with an MYB-bHLH-WD40 complex to mediate ethylene-induced ectopic root hair formation in Arabidopsis. Proceedings of the National Academy of Sciences, USA 118: e2110004118.
Qu F, Xiang Z, Zhang Y, Li J, Xiao S, Zhang Y, Mao F, Ma H, Yu Z. 2016. A novel p38 MAPK indentified from Crassostrea hongkongensis and its involvement in host response to immune challenges. Molecular Immunology 79: 113-124.
Rymen B, Kawamura A, Schäfer S, Breuer C, Iwase A, Shibata M, Ikeda M, Mitsuda N, Koncz C, Ohme-Takagi M et al. 2017. ABA suppresses root hair growth via the OBP4 transcriptional regulator. Plant Physiology 173: 1750-1762.
Smirnoff N, Wheeler GL. 2000. Ascorbic acid in plants: biosynthesis and function. Critical Reviews in Biochemistry and Molecular Biology 35: 291-314.
Sodeyama T, Nishikawa H, Harai K, Takeshima D, Sawa Y, Maruta T, Ishikawa T. 2021. The d-mannose/l-galactose pathway is the dominant ascorbate biosynthetic route in the moss Physcomitrium patens. The Plant Journal 107: 1724-1738.
Thirumalaikumar VP, Devkar V, Mehterov N, Ali S, Ozgur R, Turkan I, Mueller-Roeber B, Balazadeh S. 2018. NAC transcription factor JUNGBRUNNEN1 enhances drought tolerance in tomato. Plant Biotechnology Journal 16: 354-366.
Wang Y, Hou Y, Qiu J, Wang H, Wang S, Tang L, Tong X, Zhang J. 2020. Abscisic acid promotes jasmonic acid biosynthesis via a ‘SAPK10-bZIP72-AOC’ pathway to synergistically inhibit seed germination in rice (Oryza sativa). New Phytologist 228: 1336-1353.
Wen X, Jiao L, Tan H. 2022. MAPK/ERK pathway as a central regulator in vertebrate organ regeneration. International Journal of Molecular Sciences 23: 1464.
Wu MB, Xu X, Hu XW, Liu YD, Cao HH, Helen C, Gong ZH, Yuan YJ, Luo YQ, Feng BH et al. 2020. SlMYB72 regulates the metabolism of chlorophylls, carotenoids, and flavonoids in tomato fruit. Plant Physiology 183: 854-868.
Xu X, Zhang Q, Gao X, Wu G, Wu M, Yuan Y, Zheng X, Gong Z, Hu X, Gong M et al. 2022. Auxin and abscisic acid antagonistically regulate ascorbic acid production via the SlMAPK8-SlARF4-SlMYB11 module in tomato. Plant Cell 34: 4409-4427.
Yang X, Gabuzda D. 1998. Mitogen-activated protein kinase phosphorylates and regulates the HIV-1 Vif protein. Journal of Biological Chemistry 273: 29879-29887.
Yu C, Yan M, Dong H, Luo J, Ke Y, Guo A, Chen Y, Zhang J, Huang X. 2021. Maize bHLH55 functions positively in salt tolerance through modulation of AsA biosynthesis by directly regulating GDP-mannose pathway genes. Plant Science 302: 110676.
Yu Y, Wang J, Li S, Kakan X, Zhou Y, Miao Y, Wang FF, Qin H, Huang R. 2019. Ascorbic acid integrates the antagonistic modulation of ethylene and abscisic acid in the accumulation of reactive oxygen species. Plant Physiology 179: 1861-1875.
Yuan Y, Xu X, Luo Y, Gong Z, Hu X, Wu M, Liu Y, Yan F, Zhang X, Zhang W et al. 2021. R2R3 MYB-dependent auxin signalling regulates trichome formation, and increased trichome density confers spider mite tolerance on tomato. Plant Biotechnology Journal. 19: 138-152.
Zhang H, Xiang Y, He N, Liu X, Liu H, Fang L, Zhang F, Sun X, Zhang D, Li X et al. 2020. Enhanced vitamin C production mediated by an ABA-induced PTP-like nucleotidase improves plant drought tolerance in Arabidopsis and maize. Molecular Plant 13: 760-776.
Zhang S, Huang L, Yan A, Liu Y, Liu B, Yu C, Zhang A, Schiefelbein J, Gan Y. 2016. Multiple phytohormones promote root hair elongation by regulating a similar set of genes in the root epidermis in Arabidopsis. Journal of Experimental Botany 67: 6363-6372.
Zhao L, Yan J, Xiang Y, Sun Y, Zhang A. 2021. ZmWRKY104 transcription factor phosphorylated by ZmMPK6 functioning in ABA-induced antioxidant defense and enhance drought tolerance in maize. Biology 10: 893.
Zhao M, Li J, Zhu L, Chang P, Li L, Zhang L. 2019. Identification and characterization of MYB-bHLH-WD40 regulatory complex members controlling anthocyanidin biosynthesis in blueberry fruits development. Genes 10: 496.
Zheng X, Yuan Y, Huang B, Hu X, Tang Y, Xu X, Wu M, Gong Z, Luo Y, Gong M et al. 2022. Control of fruit softening and Ascorbic acid accumulation by manipulation of SlIMP3 in tomato. Plant Biotechnology Journal 20: 1213-1225.

Auteurs

Xin Xu (X)

Key Laboratory of Plant Hormones and Development Regulation of Chongqing, School of Life Sciences, Chongqing University, Chongqing, 400044, China.

Baowen Huang (B)

Key Laboratory of Plant Hormones and Development Regulation of Chongqing, School of Life Sciences, Chongqing University, Chongqing, 400044, China.

Xu Fang (X)

Key Laboratory of Plant Hormones and Development Regulation of Chongqing, School of Life Sciences, Chongqing University, Chongqing, 400044, China.

Qiongdan Zhang (Q)

Key Laboratory of Plant Hormones and Development Regulation of Chongqing, School of Life Sciences, Chongqing University, Chongqing, 400044, China.

Tiancheng Qi (T)

Key Laboratory of Plant Hormones and Development Regulation of Chongqing, School of Life Sciences, Chongqing University, Chongqing, 400044, China.

Min Gong (M)

Key Laboratory of Plant Hormones and Development Regulation of Chongqing, School of Life Sciences, Chongqing University, Chongqing, 400044, China.

Xianzhe Zheng (X)

Key Laboratory of Plant Hormones and Development Regulation of Chongqing, School of Life Sciences, Chongqing University, Chongqing, 400044, China.

Mengbo Wu (M)

Key Laboratory of Plant Hormones and Development Regulation of Chongqing, School of Life Sciences, Chongqing University, Chongqing, 400044, China.

Yongfei Jian (Y)

Key Laboratory of Plant Hormones and Development Regulation of Chongqing, School of Life Sciences, Chongqing University, Chongqing, 400044, China.

Jie Deng (J)

Key Laboratory of Plant Hormones and Development Regulation of Chongqing, School of Life Sciences, Chongqing University, Chongqing, 400044, China.

Yulin Cheng (Y)

Key Laboratory of Plant Hormones and Development Regulation of Chongqing, School of Life Sciences, Chongqing University, Chongqing, 400044, China.

Zhengguo Li (Z)

Key Laboratory of Plant Hormones and Development Regulation of Chongqing, School of Life Sciences, Chongqing University, Chongqing, 400044, China.

Wei Deng (W)

Key Laboratory of Plant Hormones and Development Regulation of Chongqing, School of Life Sciences, Chongqing University, Chongqing, 400044, China.

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